Rapid transmitter release at synapses depends on the close proximity of voltage-gated calcium channels (VGCCs). In mechanosensory hair cells of the vertebrate inner ear, dihydropyridine-sensitive VGCCs may be preferentially expressed at release sites to support transmitter release. In support of this hypothesis we have found that whole-cell current through VGCCs covaried with afferent innervation density among hair cells of the chick's basilar papilla (the avian analog of the mammalian Organ of Corti). The size as well as number of presynaptic dense bodies (PDBs) around which transmitter vesicles cluster varied systematically among equivalent populations of hair cells examined with electron microscopy. The total number of VGCCs was correlated with total release area (PDB cross-sectional area x the number of PDBs) among neurally located (tall) hair cells. Abneural, short hair cells with little or no afferent contact expressed a low number of VGCCs independent of release area. The implication is that hair cells augment calcium channel expression by adding release sites and by making release sites larger. This suggests further that aspects of hair cell excitability, such as electrical tuning, could depend on the synaptic architecture of each cell.